Growth‐chemical defence‐metabolomic expression trade‐off is relaxed as soil nutrient availability increases for a tropical passion vine

Abstract

Abstract Abiotic resource limitation presents organisms with a dilemma about how to use resources when they become available. Characterizing how resource allocation affects investment in growth or defensive traits that affect organismal survival strategies allows us to understand the environmental contexts in which species interact. Our goal was to measure how macronutrient availability drives nitrogen and phosphorus allocation towards functional growth and defensive chemical traits of the Neotropical passion vine, Passiflora biflora. We investigated this question with a paired field study in La Selva, Costa Rica and a full factorial greenhouse experiment to determine whether the concentration of a key secondary chemical defence is driven by nitrogen availability. We correlated defensive chemical concentration with soil nitrogen availability in naturally occurring plants, measured the effects of nitrogen and phosphorus availability on growth and secondary chemical defence traits in the greenhouse and characterized the P. biflora leaf metabolome to assess how nutrient availability affected shifts in metabolism related to plant fitness. We found that nutrient allocation increased the magnitude of both growth and defence traits. Increased nitrogen availability resulted in higher concentrations of toxic leaf secondary chemicals, longer vines, greater biomass and more leaves with a superior ability to capture sunlight. In addition, plants from high nitrogen environments had metabolomes with significantly greater secondary metabolite richness and biochemical pathway diversity, as well as increases in the number of metabolites from several chemical classes related to basic cell function and defence. Nutrient availability had no significant effect on the richness and diversity of primary metabolites involved in basic cell functions. A direct comparison of the relative strength of quantitative growth and secondary defence traits indicated that P. biflora favours nutrient allocation to growth at low nitrogen levels but invests in both strategies more evenly as nitrogen availability increases. These findings lead us to predict that passion vines are better prepared to tolerate and resist herbivory when nutrients are plentiful and experience a trade‐off between growth and chemical defence against natural enemies when they are scarce. These findings are consistent with both the ‘escape’ and ‘defend’ syndromes that are often used to describe tropical plant survival strategies. This is one of the only studies to measure nutrient allocation in vines, a group comprising a significant percentage of global plant diversity. Moreover, this work demonstrated the power of leveraging untargeted metabolomics to characterize how nutrient addition affects plant growth and defence, highlighting its potential for understanding functional trait variation. Read the free Plain Language Summary for this article on the Journal blog.